Woronin bodies, their impact on stress resistance and virulence of the pathogenic mould Aspergillus fumigatus and their anchoring at the septal pore of filamentous Ascomycota

Molecular Microbiology

Volumn 89, Issue 5, 2013, Pages 857-871

  Beck, Julia ^a   Echtenacher, Bernd ^b   Ebel, Frank ^a,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c German Center for Infection Research   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; HEXA PROTEIN; LAH PROTEIN; POLYHISTIDINE; UNCLASSIFIED DRUG;

ARTICLE; ASCOMYCETES; ASPERGILLUS FUMIGATUS; CELL ANCHORAGE; CELL FUNCTION; CELLULAR STRESS RESPONSE; CYTOARCHITECTURE; FILAMENTOUS ASCOMYCOTA; FUNGAL CELL WALL; FUNGAL GENE; FUNGAL VIRULENCE; MOLECULAR DYNAMICS; NEUROSPORA CRASSA; NONHUMAN; PEZIZOMYCOTINA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN MOTIF; PROTEIN TARGETING; WORONIN BODY;

ASCOMYCOTA; ASPERGILLUS FUMIGATUS; FUNGI; PEZIZOMYCOTINA;

ASPERGILLUS FUMIGATUS; CELL WALL; FUNGAL PROTEINS; ORGANELLES; PROTEIN BINDING; STRESS, PHYSIOLOGICAL; VIRULENCE;

EID: 84883201647     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12316     Document Type: Article

References (39)

1. Beck, J., and Ebel, F. (2013) Characterization of the major Woronin body protein HexA of the human pathogenic mold Aspergillus fumigatus. Int J Med Microbiol 303: 90-97.
2. Beck, J., Wagener, J., and Ebel, F. (2013) The septal cell wall of filamentous fungi. In The Fungal Cell Wall. Manuel Mora-Montes, H. (ed.). New York: Nova Science Publishers, pp. 129-142.
3. Berns, M.W., Aist, J.R., Wright, W.H., and Liang, H. (1992) Optical trapping in animal and fungal cells using a tunable, near-infrared titanium-sapphire laser. Exp Cell Res 198: 375-378.
4. Bleichrodt, R.J., van Veluw, G.J., Recter, B., Maruyama, J., Kitamoto, K., and Wösten, H.A. (2012) Hyphal heterogeneity in Aspergillus oryzae is the result of dynamic closure of septa by Woronin bodies. Mol Microbiol 86: 1334-1344.
5. Bouzani, M., Ok, M., McCormick, A., Ebel, F., Kurzai, O., Morton, C.O., etal. (2011) Human NK cells display important antifungal activity against Aspergillus fumigatus, which is directly mediated by IFN-γ release. J Immunol 187: 1369-1376.
6. Brakhage, A.A., Bruns, S., Thywissen, A., Zipfel, P.F., and Behnsen, J. (2010) Interaction of phagocytes with filamentous fungi. Curr Opin Microbiol 13: 409-415.
7. Collinge, A.J., and Markham, P. (1985) Woronin bodies rapidly plug septal pores of severed Penicillium chrysogenum hyphae. Exp Mycol 9: 80-95.
8. Curach, N.C., Te'o, V.S., Gibbs, M.D., Bergquist, P.L., and Nevalainen, K.M. (2004) Isolation, characterization and expression of the hex1 gene from Trichoderma reesei. Gene 331: 133-140.
9. Diamond, R.D., Krzesicki, R., Epstein, B., and Jao, W. (1978) Damage to hyphal forms of fungi by human leukocytes in vitro. A possible host defense mechanism in aspergillosis and mucormycosis. Am J Pathol 91: 313-328.
10. Fleissner, A., and Glass, N.L. (2007) SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Eukaryot Cell 6: 84-94.
11. Gould, S.J., Keller, G.A., Hosken, N., Wilkinson, J., and Subramani, S. (1989) A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108: 1657-1664.
12. Jedd, G. (2011) Fungal evo-devo: organelles and multicellular complexity. Trends Cell Biol 21: 12-19.
13. Jedd, G., and Chua, N.H. (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2: 226-231.
14. Kim, K.H., Willger, S.D., Park, S.W., Puttikamonkul, S., Grahl, N., Cho, Y., etal. (2009) TmpL, a transmembrane protein required for intracellular redox homeostasis and virulence in a plant and an animal fungal pathogen. PLoS Pathog 5: e1000653.
15. Kirk, P.M., Cannon, P.F., David, J.C., and Stalpers, J.A. (2001) Ainsworth and Bisby's Dictionary of the Fungi, 9th edn. Wallingford, UK: CAB International.
16. Kotz, A., Wagener, J., Engel, J., Routier, F.H., Echtenacher, B., Jacobsen, I., etal. (2010) Approaching the secrets of N-glycosylation in Aspergillus fumigatus: characterization of the AfOch1 protein. PLoS ONE 5: e15729.
17. Krappmann, S., Sasse, C., and Braus, G.H. (2006) Gene targeting in Aspergillus fumigatus by homologous recombination is facilitated in a nonhomologous end-joining-deficient genetic background. Eukaryot Cell 5: 212-215.
18. Lai, J., Koh, C.H., Tjota, M., Pieuchot, L., Raman, V., Chandrababu, K.B., etal. (2012) Intrinsically disordered proteins aggregate at fungal cell-to-cell channels and regulate intercellular connectivity. Proc Natl Acad Sci USA 109: 15781-15786.
19. Latgé, J.P. (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310-350.
20. Lew, R.R. (2005) Mass flow and pressure-driven hyphal extension in Neurospora crassa. Microbiology 151: 2685-2692.
21. Lin, S.J., Schranz, J., and Teutsch, S.M. (2001) Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 32: 358-366.
22. Liu, F., Ng, S.K., Lu, Y., Low, W., Lai, J., and Jedd, G. (2008) Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 180: 325-339.
23. Liu, F., Lu, Y., Pieuchot, L., Dhavale, T., and Jedd, G. (2011) Import oligomers induce positive feedback to promote peroxisome differentiation and control organelle abundance. Dev Cell 21: 457-468.
24. McCormick, A., Loeffler, J., and Ebel, F. (2010) Aspergillus fumigatus: contours of an opportunistic human pathogen. Cell Microbiol 12: 1535-1543.
25. McCormick, A., Jacobsen, I.D., Broniszewska, M., Beck, J., Heesemann, J., and Ebel, F. (2012) The two-component sensor kinase TcsC and its role in stress resistance of the human-pathogenic mold Aspergillus fumigatus. PLoS ONE 7: e38262.
26. Maruyama, J., Juvvadi, P.R., Ishi, K., and Kitamoto, K. (2005) Three-dimensional image analysis of plugging at the septal pore by Woronin body during hypotonic shock inducing hyphal tip bursting in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 331: 1081-1088.
27. Maruyama, J., Escaño, C.S., and Kitamoto, K. (2010) AoSO protein accumulates at the septal pore in response to various stresses in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 391: 868-873.
28. Momany, M., Richardson, E.A., Van Sickle, C., and Jedd, G. (2002) Mapping Woronin body position in Aspergillus nidulans. Mycologia 94: 260-266.
29. Ng, S.K., Liu, F., Lai, J., Low, W., and Jedd, G. (2009) A tether for Woronin body inheritance is associated with evolutionary variation in organelle positioning. PLoS Genet 5: e1000521.
30. Plamann, M. (2009) Cytoplasmic streaming in Neurospora: disperse the plug to increase the flow? PLoS Genet 5: e1000526.
31. Punt, P.J., and van den Hondel, V.A. (1992) Transformation of filamentous fungi based on hygromycin B and phleomycin resistance markers. Methods Enzymol 216: 447-457.
32. Rohde, M., Schwienbacher, M., Nikolaus, T., Heesemann, J., and Ebel, F. (2002) Detection of early phase specific surface appendages during germination of Aspergillus fumigatus conidia. FEMS Microbiol Lett 206: 99-105.
33. Rokka, A., Antonenkov, V.D., Soininen, R., Immonen, H.L., Pirilä, P.L., Bergmann, U., etal. (2009) Pxmp2 is a channel-forming protein in mammalian peroxisomal membrane. PLoS ONE 4: e5090.
34. Schmidt, S., Tramsen, L., Hanisch, M., Latgé, J.P., Huenecke, S., Koehl, U., and Lehrnbecher, T. (2011) Human natural killer cells exhibit direct activity against Aspergillus fumigatus hyphae, but not against resting conidia. J Infect Dis 203: 430-435.
35. Soundararajana, S., Jedd, G., Lia, X., Ramos-Pamploñaa, M., Chuab, N.H., and Naqvia, N.I. (2004) Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 16: 1564-1574.
36. Tenney, K., Hunt, I., Sweigard, J., Pounder, J.I., McClain, C., Bowman, E.J., and Bowman, B.J. (2000) Hex-1, a gene unique to filamentous fungi, encodes the major protein of the Woronin body and functions as a plug for septal pores. Fungal Genet Biol 31: 205-217.
37. Verweij, P.E., Kema, G.H., Zwaan, B., and Melchers, W.J. (2012) Triazole fungicides and the selection of resistance to medical triazoles in the opportunistic mould Aspergillus fumigatus. Pest Manag Sci 69: 165-170.
38. Woronin, M. (1864) Entwicklungsgeschichte des Ascobolus pucherrimus Cr. und einiger Pezizen. Abh Senkenb Naturforsch 5: 355-344.
39. Yuan, P., Jedd, G., Kumaran, D., Swaminathan, S., Shio, H., Hewitt, D., etal. (2003) A HEX-1 crystal lattice required for Woronin body function in Neurospora crassa. Nat Struct Biol 10: 264-270.